16
Views
199
CrossRef citations to date
0
Altmetric
Research Article

Human Fibroblast Commitment to a Senescence-Like State in Response to Histone Deacetylase Inhibitors Is Cell Cycle Dependent

, , , &
Pages 5210-5218 | Received 29 Jan 1996, Accepted 16 May 1996, Published online: 29 Mar 2023

REFERENCES

  • Allsopp, R. C., H. Vaziri, C. Patterson, S. Goldstein, E. V. Younglai, A. B. Futcher, C. W. Greider, and C. B. Harley. 1992. Telomere length predicts replicative capacity of human fibroblasts. Proc. Natl. Acad. Sci. USA 89:10114–10118.
  • Annunziato, A. T., and R. L. Seale. 1983. Histone deacetylation is required for the maturation of newly replicated chromatin. J. Biol. Chem. 258:12675–12684.
  • Atadja, P. W., K. F. Stringer, and K. T. Riabowol. 1994. Loss of serum response element-binding activity and hyperphosphorylation of serum response factor during cellular aging. Mol. Cell. Biol. 14:4991–4999.
  • Bayreuther, K., H. P. Rodemann, R. Hommel, K. Dittmann, M. Albiez, and P. I. Francz. 1988. Human skin fibroblasts in vitro differentiate along a terminal cell lineage. Proc. Natl. Acad. Sci. USA 85:5112–5116.
  • Bischoff, F. Z., S. O. Yim, S. Pathak, G. Grant, M. J. Siciliano, B. C. Giovanella, L. C. Strong, and M. A. Tainsky. 1990. Spontaneous abnormalities in normal fibroblasts from patients with Li-Fraumeni cancer syndrome: aneuploidy and immortalization. Cancer Res. 50:7979–7984.
  • Boffa, L. C., M. R. Mariani, and M. I. Parker. 1994. Selective hypermethy-lation of transcribed nucleosomal DNA by sodium butyrate. Exp. Cell Res. 2:420–423.
  • Boyd, A. W., and D. Metcalf. 1984. Induction of differentiation in HL60 leukaemic cells: a cell cycle dependent all-or-none event. Leukemia Res. 8:27–43.
  • Brownell, J. E., J. Zhou, T. Ranalli, R. Kobayashi, D. G. Edmondson, S. Y. Roth, and C. D. Allis. 1996. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84:843–851.
  • Campisi, J. Personal communication.
  • Candido, E. P., R. Reeves, and J. R. Davie. 1978. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell 14:105–113.
  • Catania, J., and D. S. Fairweather. 1991. DNA methylation and cellular aging. Mutat. Res. 256:283–293.
  • Cattanach, B. M. 1974. Position effect variegation in the mouse. Genet. Res. 23:291–306.
  • Chen, Q., and B. N. Ames. 1994. Senescence-like growth arrest induced by hydrogen peroxide in human diploid fibroblast F65 cells. Proc. Natl. Acad. Sci. USA 91:4130–4134.
  • Chen, Q., A. Fischer, J. D. Reagan, L. J. Yan, and B. N. Ames. 1995. Oxidative DNA damage and senescence of human diploid fibroblast cells. Proc. Natl. Acad. Sci. USA 92:4337–4341.
  • Cook, K. R., and G. H. Karpen. 1994. A rosy future for heterochromatin. Proc. Natl. Acad. Sci. USA 91:5219–5221.
  • Cosgrove, D. E., and G. S. Cox. 1990. Effects of sodium butyrate and 5-aza-cytidine on DNA methylation in human tumor cell lines: variable response to drug treatment and withdrawal. Biochim. Biophys. Acta 1087:80–87.
  • Cristofalo, V. J. 1972. Animal cell cultures as a model system for the study of aging. Adv. Gerontol. Res. 4:45–79.
  • Cristofalo, V. J., and R. J. Pignolo. 1993. Replicative senescence of human fibroblast-like cells in culture. Physiol. Rev. 73:617–638.
  • Csordas, A. 1990. On the biological role of histone acetylation. Biochem. J. 265:23–38.
  • Dell’Orco, R. T., J. G. Mertens, and P. F. Kruse, Jr. 1973. Doubling potential, calendar time, and senescence of human diploid cells in culture. Exp. Cell Res. 77:356–360.
  • Dimri, G. P., X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E. E. Medrano, M. Linskens, I. Rubelj, O. Pereira-Smith, M. Peacocke, and J. Campisi. 1995. A novel biomarker identifies senescent human cells in culture and aging skin in vivo. Proc. Natl. Acad. Sci. USA 92:9363–9367.
  • Dulic, V., L. F. Drullinger, E. Lees, S. I. Reed, and G. H. Stein. 1993. Altered regulation of G1 cyclins in senescent human diploid fibroblasts: accumulation of inactive cyclin E-Cdk2 and cyclin D1-Cdk2 complexes. Proc. Natl. Acad. Sci. USA 90:11034–11038.
  • Dunaief, J. L., B. E. Strober, S. Guha, P. A. Khavari, K. Alin, J. Luban, M. Begemann, G. R. Crabtree, and S. P. Goff. 1994. The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest. Cell 79:119–130.
  • Fairweather, D. S., M. Fox, and G. P. Margison. 1987. The in vitro lifespan of MRC-5 cells is shortened by 5-azacytidine-induced demethylation. Exp. Cell Res. 168:153–159.
  • Foss, F. M., A. Veillette, O. Sartor, N. Rosen, and J. B. Bolen. 1989. Alterations in the expression of pp60c-src and p56lck associated with butyrate-induced differentiation of human colon carcinoma cells. Oncogene Res. 5:13–23.
  • Giordano, T., T. H. Howard, J. Coleman, K. Sakamoto, and B. H. Howard. 1990. Isolation of a population of transiently transfected quiescent and senescent cells by magnetic affinity cell sorting. Exp. Cell Res. 192:193–197.
  • Goldstein, S. 1990. Replicative senescence: the human fibroblast comes of age. Science 249:1129–1133.
  • Goldstein, S., and D. P. Singal. 1974. Senescence of cultured human fibro-blasts: mitotic versus metabolic time. Exp. Cell Res. 88:359–364.
  • Gorman, C. M., B. H. Howard, and R. Reeves. 1983. Expression of recom-binant plasmids in mammalian cells is enhanced by sodium butyrate. Nucleic Acids Res. 11:7631–7648.
  • Gorman, S. D., and V. J. Cristofalo. 1985. Reinitiation of cellular DNA synthesis in BrdU-selected nondividing senescent WI-38 cells by simian virus 40 infection. J. Cell. Physiol. 125:122–126.
  • Grove, G. L., and R. B. Mitchell. 1974. DNA microdensitometry as a measure of cycling-non-cycling activity in aged human diploid cells in culture. Mech. Ageing Dev. 3:235–240.
  • Hara, E., H. Tsurui, A. Shinozaki, S. Nakada, and K. Oda. 1991. Cooperative effect of antisense-Rb and antisense-p53 oligomers on the extension of life span in human diploid fibroblasts, TIG-1. Biochem. Biophys. Res. Com-mun. 179:528–534.
  • Hara, E., T. Yamaguchi, H. Nojima, T. Ide, J. Campisi, H. Okayama, and K. Oda. 1994. Id-related genes encoding helix-loop-helix proteins are required for G1 progression and are repressed in senescent human fibroblasts. J. Biol. Chem. 269:2139–2145.
  • Harley, C. B., A. B. Futcher, and C. W. Greider. 1990. Telomeres shorten during ageing of human fibroblasts. Nature (London) 345:458–460.
  • Hastie, N. D., M. Dempster, M. G. Dunlop, A. M. Thompson, D. K. Green, and R. C. Allshire. 1990. Telomere reduction in human colorectal carcinoma and with ageing. Nature (London) 346:866–868.
  • Hayflick, L., and P. S. Moorehead. 1961. The serial cultivation of human diploid cell strains. Exp. Cell. Res. 25:585–621.
  • Hearn, M. G., A. Hedrick, T. A. Grigliatti, and B. T. Wakimoto. 1991. The effect of modifiers of position-effect variegation on the variegation of het-erochromatic genes in Drosophila melanogaster. Genetics 128:785–797.
  • Henikoff, S. 1994. A reconsideration of the mechanism of position effect. Genetics 138:1–5.
  • Ho, S. B., P.-S. Yan, R. Dahiya, B. A. Neuschwander-Tetri, C. Basbaum, and Y. S. Kim. 1994. Stable differentiation of a human colon adenocarcinoma cell line by sodium butyrate is associated with multidrug resistance. J. Cell. Physiol. 160:213–226.
  • Ide, T., Y. Tsuji, S. Ishibashi, and Y. Mitsui. 1983. Reinitiation of host DNA synthesis in senescent human diploid cells by infection with simian virus 40. Exp. Cell Res. 143:343–349.
  • Jeppesen, P., and B. M. Turner. 1993. The inactive X chromosome in female mammals in distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell 74:281–289.
  • Kennedy, B. K., N. R. Austriaco, J. Zhang, and L. Guarente. 1995. Mutation in the silencing gene SIR4 can delay aging in S. cerevisiae. Cell 80:485–496.
  • Koonin, E. V., S. Zhou, and J. C. Lucchesi. 1995. The chromo superfamily: new members, duplication of the chromo domain and possible role in delivering transcription factors to chromatin. Nucleic Acids Res. 23:4229–4233.
  • Kruh, J. 1982. Effects of sodium butyrate, a new pharmacological agent, on cells in culture. Mol. Cell. Biochem. 42:65–82.
  • Laurenson, P., and J. Rine. 1992. Silencers, silencing, and heritable tran-scriptional states. Microbiol. Rev. 56:543–560.
  • Marks, P. A., V. M. Richon, H. Kiyokawa, and R. A. Rifkind. 1994. Inducing differentiation of transformed cells with hybrid polar compounds: a cell cycle-dependent process. Proc. Natl. Acad. Sci. USA 91:10251–10254.
  • Marks, P. A., and R. A. Rifkind. 1978. Erythroleukemic differentiation. Annu. Rev. Biochem. 47:419–448.
  • Martin, C. C., and R. McGowan. 1995. Genotype-specific modifiers of trans-gene methylation and expression in the zebrafish, Danio rerio. Genet. Res. 65:21–28.
  • Martin, G. M., M. S. Sprague, T. H. Norwood, and W. R. Pendergrass. 1974. Clonal selection, attenuation and differentiation in an in vitro model of hyperplasia. Am. J. Pathol. 74:137–150.
  • Migeon, B. R., J. Axelman, and A. H. Beggs. 1988. Effect of ageing on reactivation of the human X-linked HPRT locus. Nature (London) 335:93–96.
  • Morrow, C. S., M. Nakagawa, M. E. Goldsmith, M. J. Madden, and K. H. Cowen. 1994. Reversible transcriptional activation of mdr1 by sodium bu-tyrate treatment of human colon cancer cells. J. Biol. Chem. 269:10739–10746.
  • Mottus, R., R. Reeves, and T. A. Grigliatti. 1980. Butyrate suppression of position-effect variegation in Drosophila melanogaster. Mol. Gen. Genet. 178:465–469.
  • Noda, A., Y. Ning, S. F. Venable, O. M. Pereira-Smith, and J. R. Smith. 1994. Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211:90–98.
  • Norwood, T. H., and J. R. Smith. 1985. The cultured fibroblast-like cell as a model for the study of aging, p. 291–321. In C. E. Finch and E. L. Schneider (ed.), Handbook of the biology of aging. Van Nostrand Reinhold, New York.
  • Ogryzko, V. V., T. H. Hirai, C. E. Shih, and B. H. Howard. 1994. Dissociation of retinoblastoma gene protein hyperphosphorylation and commitment to enter S phase. J. Virol. 68:3724–3732.
  • Olovnikov, A. M. 1973. A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol. 41:181–190.
  • Parker, M. I., J. B. de Haan, and W. Gevers. 1986. DNA hypermethylation in sodium butyrate-treated WI-38 fibroblasts. J. Biol. Chem. 261:2786–2790.
  • Peacocke, M., and J. Campisi. 1991. Cellular senescence—a reflection of normal growth control, differentiation, or aging. J. Cell. Biochem. 45:147–155.
  • Pillus, L., and J. Rine. 1989. Epigenetic inheritance of transcriptional states in S. cerevisiae. Cell 59:637–647.
  • Pirrotta, V., and L. Rastelli. 1994. white gene expression, repressive chro-matin domains and homeotic gene regulation in Drosophila. Bioessays 16:549–556.
  • Quinn, L. S., T. H. Norwood, and M. Nameroff. 1988. Myogenic stem cell commitment probability remains constant as a function of organismal and mitotic age. J. Cell. Physiol. 134:324–336.
  • Reuter, G., and P. Spierer. 1992. Position effect variegation and chromatin proteins. Bioessays 14:605–612.
  • Riabowol, K., J. Schiff, and M. Z. Gilman. 1992. Transcription factor AP-1 activity is required for initiation of DNA synthesis and is lost during cellular aging. Proc. Natl. Acad. Sci. USA 89:157–161.
  • Rivier, D. H., and J. Rine. 1992. Silencing: the establishment and inheritance of stable, repressed transcription states. Curr. Opin. Genet. Dev. 2:286–292.
  • Roberts, T. W., and J. R. Smith. 1980. The proliferative potential of chick embryo fibroblasts: population doublings vs. time in culture. Cell Biol. Int. Rep. 4:1057–1063.
  • Sakamoto, K., T. Howard, V. Ogryzko, N.-Z. Xu, C. C. Corsico, J. H. Jones, and B. H. Howard. 1993. Relative mitogenic activities of wild-type and retinoblastoma binding-defective SV40 T antigens in serum-deprived and senescent human diploid fibroblasts. Oncogene 8:1887–1893.
  • Schanz, S., and P. Steinbach. 1989. Investigation of the “variable spreading” of X inactivation into a translocated autosome. Hum. Genet. 82:244–248.
  • Sealy, L., and R. Chalkley. 1978. The effect of sodium butyrate on histone modification. Cell 14:115–121.
  • Seshadri, T., and J. Campisi. 1990. Repression of c-fos transcription and an altered genetic program in senescent human fibroblasts. Science 247:205–209.
  • Shaffer, C. D., L. L. Wallrath, and S. C. Elgin. 1993. Regulating genes by packaging domains: bits of heterochromatin in euchromatin? Trends Genet. 9:35–37.
  • Shay, J. W., O. M. Pereira-Smith, and W. E. Wright. 1991. A role for both RB and p53 in the regulation of human cellular senescence. Exp. Cell Res. 196:33–39.
  • Simon, J., A. Chiang, W. Bender, M. J. Shimell, and M. O’Connor. 1993. Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev. Biol. 158:131–144.
  • Sinclair, D. A., A. A. Ruddell, J. K. Brock, N. J. Clegg, V. K. Lloyd, and T. A. Grigliatti. 1992. A cytogenetic and genetic characterization of a group of closely linked second chromosome mutations that suppress position-effect variegation in Drosophila melanogaster. Genetics 130:333–344.
  • Smith, J. R., and D. W. Lincoln. 1984. Aging of cells in culture. Int. Rev. Cytol. 89:151–177.
  • Sohal, R. S., and R. G. Allen. 1990. Oxidative stress as a causal factor in differentiation and aging: a unifying hypothesis. Exp. Gerontol. 25:499–522.
  • Stadtman, E. R. 1992. Protein oxidation and aging. Science 257:1220–1224.
  • Stein, G. H., M. Beeson, and L. Gordon. 1990. Failure to phosphorylate the retinoblastoma gene product in senescent human fibroblasts. Science 249:666–669.
  • Stein, G. H., L. F. Drullinger, R. S. Robetorye, O. M. Pereirasmith, and J. R. Smith. 1991. Senescent cells fail to express cdc2, cycA, and cycB in response to mitogen stimulation. Proc. Natl. Acad. Sci. USA 88:11012–11016.
  • Szekely, L., E. Uzvolgyi, W. Q. Jiang, M. Durko, K. G. Wiman, G. Klein, and J. Sumegi. 1991. Subcellular localization of the retinoblastoma protein. Cell Growth Differ. 2:287–295.
  • Thomas, N. S. B., L. C. Burke, A. Bybee, and D. C. Linch. 1991. The phosphorylation state of the retinoblastoma (RB) protein in G0/G1 is dependent on growth status. Oncogene 6:317–322.
  • Tsuji, Y., T. Ide, and S. Ishibashi. 1983. Correlation between the presence of T-antigen and the reinitiation of host DNA synthesis in senescent human diploid fibroblasts after SV40 infection. Exp. Cell Res. 144:165–169.
  • Tsukada, M., Y. Wada, N. Hamade, H. Masuda, and A. Koizumi. 1991. Stable lyonization of X-linked pgk-1 gene during aging in normal tissues and tumors of mice carrying Searle’s translocation. J. Gerontol. 46:B213–B216.
  • Vidali, G., L. C. Boffa, E. M. Bradbury, and V. G. Allfrey. 1978. Butyrate suppression of histone deacetylation leads to accumulation of multiacety-lated forms of histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proc. Natl. Acad. Sci. USA 75:2239–2243.
  • von Zglinicki, T., G. Saretzki, W. Docke, and C. Lotze. 1995. Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence? Exp. Cell Res. 220:186–193.
  • Wareham, K. A., M. F. Lyon, P. H. Glenister, and E. D. Williams. 1987. Age related reactivation of an X-linked gene. Nature (London) 327:725–727.
  • Warner, H. R., J. Campisi, V. J. Cristofalo, R. A. Miller, J. Papacon-stantinou, O. Pereira-Smith, J. R. Smith, and E. Wang. 1992. Control of cell proliferation in senescent cells. J. Gerontol. 47:B185–B189.
  • Wilson, V. L., and P. A. Jones. 1983. DNA methylation decreases in aging but not in immortal cells. Science 220:1055–1057.
  • Wright, W. E., and J. W. Shay. 1992. Telomere positional effects and the regulation of cellular senescence. Trends Genet. 8:193–197.
  • Yang, L., and P. Hornsby. 1989. Dissociation of senescence-associated changes in differentiated gene expression and replicative senescence in cultured adrenocortical cells. J. Cell Sci. 94:757–768.
  • Yanishevsky, R., M. L. Mendelsohn, B. H. Mayall, and V. J. Cristofalo. 1974. Proliferative capacity and DNA content of aging human diploid cells in culture: a cytophotometric and autoradiographic analysis. J. Cell. Physiol. 84:165–170.
  • Yoshida, M., M. Kijima, M. Akita, and T. Beppu. 1990. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J. Biol. Chem. 265:17174–17179.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.